Theory suggests that effective clearance of harmful mutations requires sexual reproduction, butwhether asexuals in natural populations experience mutation accumulation as a direct consequence of asexuality remains an open question. We sequenced mitochondrial genomes from multiple sexual and asexual lineages of a New Zealand freshwater snail to evaluate whether mutation accumulation is associated with asexuality in a species where sexuals and asexuals regularly coexist. Asexuals experienced markedly higher rates of mutation accumulation relative to sexuals, which was evident even in recently derived asexual lineages. This is the first evidence that purifying selection is consistently ineffective in asexuals relative to sexual competitors in natural populations. Our results point to a direct link between asexuality and mutation accumulation, and demonstrate that increased mutation accumulation in asexuals can occur rapidly enough to differentially affect sexual vs. asexual lineages within populations.